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Library of Congress Cataloging in Publication Data
Fawcett, Don Wayne, 1917The cell.
DON W . FAWCETT. M.D.
Hersey Professor of Anatomy
Harvard Medical School
Edition of 1966 published under title: An atlas of
fine structure.
Includes bibliographical references.
2. Ultrastructure (Biology)1. Cytology -Atlases.
I. Title. [DNLM: 1. Cells- UltrastructureAtlases.
2. Cells- Physiology - Atlases. QH582 F278c]
Atlases.
QH582.F38 1981
591.8'7
80-50297
ISBN 0-7216-3584-9
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CONTRIBUTORS OF
ELECTRON MICROGRAPHS
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PREFACE
PREFACE
ably used in combination with biochemical, biophysical, and immunocytochemical
techniques. Its use has become routine and one begins to detect a decline in the number
and quality of published micrographs as other analytical methods increasingly capture
the interest of investigators. Although purely descriptive electron microscopic studies
now yield diminishing returns, a detailed knowledge of the structural organization of
cells continues to be an indispensable foundation for research on cell biology. In undertaking this second edition I have been motivated by a desire to assemble and make
easily accessible to students and teachers some of the best of the many informative
and aesthetically pleasing transmission and scanning electron micrographs that form
the basis of our present understanding of cell structure.
The historical approach employed in the text may not be welcomed by all. In the
competitive arena of biological research today investigators tend to be interested only
in the current state of knowledge and care little about the steps by which we have
arrived at our present position. But to those of us who for the past 25 years have been
privileged to participate in one of the most exciting and fruitful periods in the long
history of morphology, the young seem to be entering the theater in the middle of an
absorbing motion picture without knowing what has gone before. Therefore, in the
introduction to each organelle, I have tried to identify, in temporal sequence, a few of
the major contributors to our present understanding of its structure and function. In
venturing to do this I am cognizant of the hazards inherent in making judgments of
priority and significance while many of the dramatis personae are still living. My
apologies to any who may feel that their work has not received appropriate recognition.
It is my hope that for students and young investigators entering the field, this book
will provide a useful introduction to the architecture of cells and for teachers of cell
biology a guide to the literature and a convenient source of illustrative material. The
sectional bibliographies include references to many reviews and research papers that
are not cited in the text. It is believed that these will prove useful to those readers who
wish to go into the subject more deeply.
The omission of magnifications for each of the micrographs will no doubt draw
some criticism. Their inclusion was impractical since the original negatives often
remained in the hands of the contributing microscopists and micrographs submitted
were cropped or copies enlarged to achieve pleasing composition and to focus the
reader's attention upon the particular organelle under discussion. Absence was considered preferable to inaccuracy in stated magnification. The majority of readers, I
believe, will be interested in form rather than measurement and will not miss this datum.
Assembling these micrographs illustrating the remarkable order and functional
design in the structure of cells has been a satisfying experience. I am indebted to more
than a hundred cell biologists in this country and abroad who have generously responded to my requests for exceptional micrographs. It is a source of pride that nearly
half of the contributors were students, fellows or colleagues in the Department of
Anatomy at Harvard Medical School at some time in the past 20 years. I am grateful
for their stimulation and for their generosity in sharing prints and negatives. It is a
pleasure to express my appreciation for the forbearance of my wife who has had to
communicate with me through the door of the darkroom for much of the year while I
printed the several hundred micrographs; and for the patience of Helen Deacon who
has typed and retyped the manuscript; for the skill of Peter Ley, who has made many
copy negatives to gain contrast with minimal loss of detail; and for the artistry of
Sylvia Collard Keene whose drawings embellish the text. Special thanks go to Elio
and Giuseppina Raviola who read the manuscript and offered many constructive
suggestions; and to Albert Meier and the editorial and production staff of the W. B.
Saunders Company, the publishers.
And finally I express my gratitude to the Simon Guggenheim Foundation whose
commendable policy of encouraging the creativity of the young was relaxed to support
my efforts during the later stages of preparation of this work.
The history of morphological science is in large measure a chronicle of the discovery of new preparative techniques and the development of more powerful optical
instruments. In the middle of the 19th century, improvements in the correction of
lenses for the light microscope and the introduction of aniline dyes for selective staining of tissue components ushered in a period of rapid discovery that laid the foundations of modern histology and histopathology. The decade around the turn of this
century was a golden period in the history of microscopic anatomy, with the leading
laboratories using a great variety of fixatives and combinations of dyes to produce
histological preparations of exceptional quality. The literature of that period abounds
in classical descriptions of tissue structure illustrated by exquisite lithographs. In the
decades that followed, the tempo of discovery with the light microscope slackened;
interest in innovation in microtechnique declined, and specimen preparation narrowed
to a monotonous routine of paraffin sections stained with hematoxylin and eosin.
In the middle of the 20th century, the introduction of the electron microscope
suddenly provided access to a vast area of biological structure that had previously
been beyond the reach of the compound microscope. Entirely new methods of specimen preparation were required to exploit the resolving power of this new instrument.
Once again improvement of fixation, staining, and microtomy commanded the attention of the leading laboratories. Study of the substructure of cells was eagerly pursued
with the same excitement and anticipation that attend the geographical exploration of
a new continent. Every organ examined yielded a rich reward of new structural information. Unfamiliar cell organelles and inclusions and new macromolecular components
of protoplasm were rapidly described and their function almost as quickly established.
This bountiful harvest of new structural information brought about an unprecedented
convergence of the interests of morphologists, physiologists, and biochemists; this
convergence has culminated in the unified new field of science called cell biology.
The first edition of this book (1966) appeared in a period of generous support of
science, when scores of laboratories were acquiring electron microscopes and hundreds
of investigators were eagerly turning to this instrument to extend their research to the
subcellular level. A t that time, an extensive text in this rapidly advancing field would
have been premature, but there did seem to be a need for an atlas of the ultrastructure
of cells to establish acceptable technical standards of electron microscopy and to
define and illustrate the cell organelles in a manner that would help novices in the field
to interpret their own micrographs. There is reason to believe that the first edition of
The Cell: An Atlas of Fine Structure fulfilled this limited objective.
In the 14 years since its publication, dramatic progress has been made in both the
morphological and functional aspects of cell biology. The scanning electron microscope
and the freeze-fracturing technique have been added to the armamentarium of the
miscroscopist, and it seems timely to update the book to incorporate examples of the
application of these newer methods, and to correct earlier interpretations that have not
withstood the test of time. The text has been completely rewritten and considerably
expanded. Drawings and diagrams have been added as text figures. A few of the
original transmission electron micrographs to which I have a sentimental attachment
have been retained, but the great majority of the micrographs in this edition are new.
These changes have inevitably added considerably to the length of the book and therefore to its price, but I hope these will be offset to some extent by its greater informational content.
Twenty years ago, the electron microscope was a solo instrument played by a few
virtuosos. Now it is but one among many valuable research tools, and it is most profitv
D ON W. FAWCETT
Boston, Massachusetts
CONTENTS
CONTENTS
MITOCHONDRIA ................................................................................. 410
CELL SURFACE...................................................................................
1
Cell Membrane ........................................................................................
Glycocalyx or Surface Coat .......................................................................
Basal Lamina ..........................................................................................
1
35
45
SPECIALIZATIONS O F T H E FREE SURFACE ....................................
65
Specializations for Surface Amplification......................................................
Relatively Stable Surface Specializations ......................................................
Specializations Involved in Endocytosis .......................................................
68
80
92
......................................................
Tight Junction (Zonula Occludens)..............................................................
Adhering Junction (Zonula Adherens)..........................................................
Sertoli Cell Junctions ................................................................................
Zonula Continua and Septate Junctions of Invertebrates .................................
Desmosomes ...........................................................................................
Gap Junctions (Nexuses)...........................................................................
Intercalated Discs and Gap Junctions of Cardiac Muscle ................................
124
............................................................................................
Nuclear Size and Shape ............................................................................
Chromatin...............................................................................................
Mitotic Chromosomes ...............................................................................
Nucleolus ...............................................................................................
Nucleolar Envelope ..................................................................................
Annulate Lamellae ...................................................................................
195
ENDOPLASMIC RETICULUM .............................................................
303
JUNCTIONAL SPECIALIZATIONS
NUCLEUS
Structure of Mitochondria ..........................................................................
Matrix Granules ......................................................................................
Mitochondria1 DNA and RNA ...................................................................
Division of Mitochondria ...........................................................................
Fusion of Mitochondria .............................................................................
Variations in Internal Structure ..................................................................
Mitochondria1 Inclusions ...........................................................................
Numbers and Distribution .........................................................................
414
420
424
430
438
442
464
468
LYSOSOMES ......................................................................................... 487
Multivesicular Bodies ............................................................................... 510
PEROXISOMES ..................................................................................... 515
LIPOCHROME PIGMENT .................................................................... 529
MELANIN PIGMENT ........................................................................... 537
CENTRIOLES ....................................................................................... 551
128
129
136
148
156
169
187
Centriolar Adjunct
................................................................................... 568
CILIA AND FLAGELLA ...................................................................... 575
Matrix Components of Cilia ....................................................................... 588
Aberrant Solitary Cilia .............................................................................. 594
Modified Cilia.......................................................................................... 596
Stereocilia ............................................................................................... 598
197
204
226
243
266
292
SPERM FLAGELLUM
.......................................................................... 604
Mammalian Sperm Flagellum ..................................................................... 604
Urodele Sperm Flagellum .......................................................................... 619
Insect Sperm Flagellum............................................................................. 624
CYTOPLASMIC INCLUSIONS
............................................................. 641
Glycogen ................................................................................................
Lipid ......................................................................................................
Crystalline Inclusions ...............................................................................
Secretory Products ...................................................................................
Synapses ................................................................................................
Rough Endoplasmic Reticulum ................................................................... 303
Smooth Endoplasmic Reticulum ................................................................. 330
Sarcoplasmic Reticulum ............................................................................ 353
GOLGI APPARATUS ............................................................................ 369
Role in Secretion ..................................................................................... 372
Role in Carbohydrate and Glycoprotein Synthesis ......................................... 376
Contributions to the Cell Membrane............................................................ 406
641
655
668
691
722
CYTOPLASMIC MATRIX AND CYTOSKELETON .............................. 743
vii
Microtubules ........................................................................................... 743
Cytoplasmic Filaments .............................................................................. 784
PEROXISOMES
In an early electron microscopic study of the kidney, Rhodin (1954) described
membrane-limited, spherical cytoplasmic particles 0.2 to 0.4 pm in diameter that did
not correspond to any of the traditional cell organelles. For lack of a better term, they
were called microbodies. Similar structures were soon observed in hepatic cells, but in
addition to a homogeneous, finely granular matrix these also contained an inclusion
termed the nucleoid, which in some planes of section exhibited a lamellar substructure
(Gansler and Rouiller, 1956). Noting that microbodies were more abundant in regenerating liver, Rouiller and Bernhard (1956) considered it likely that they represented
formative stages of mitochondria and that the parallel striations in the nucleoid might be
precursors of the cristae, but this interpretation gained little support.
In their studies on lysosomes, DeDuve and his coworkers developed centrifugation
procedures with improved resolving power and were able to separate from the
lysosome fraction particles that lacked the typical acid hydrolases but were rich in
d-aminoacid oxidase and catalase. It was recognized that this new class of cytoplasmic
particles probably corresponded to the "microbodies" previously described by microscopists. It was suggested that the term peroxisome was more appropriate for an
organelle in which two hydrogen peroxide-generating enzymes were associated with
catalase. This rapidly became the preferred term.
Correspondence of DeDuve's peroxisomes to microbodies was soon validated by
the demonstration that the ultrastructure of the nucleoid in the microbody was identical
to that of crystalline uricase (Hruban and Swift, 1964) and the finding that birds,
reptiles, and man - all of which are known to lack uricase - also lack nucleoids in
their hepatic microbodies (Afzelius, 1965). The nucleoids of rat hepatic microbodies
were then isolated in a high degree of purity and urate oxidase was the only enzymatic
activity detected. The isolated nucleoids consisted of parallel bundles of thick-walled,
hollow tubules (15 nm outside diameter, 5 nm inside diameter). These were precisely
arranged in a repeating pattern throughout the crystalline lattice with 10 such tubules
around longitudinal channels 20 nm in diameter. Thus in transverse sections the
nucleoids had a honeycomb pattern, and in longitudinal sections they presented an
array of alternating dark and light striations (Tsukada et al., 1966). This structure
applies only to the rat. The nucleoids of other species have a different organization.
Investigation of the origin of peroxisomes has been considerably facilitated by the
availability of experimental methods for inducing their proliferation and by a cytochemical reaction for detecting their enzymatic activity. Administration of various hypocholesterolemic drugs results in a rapid increase in hepatic microbodies (Hruban et al., 1970;
Diagrammatic reconstruction of the three-dimensional form of the nucleoid in rat hepatic peroxisomes. (From Tsukada et a]., J. Cell Biol. 28:449-460, 1966.)
5 16
PEROXISOMES
Reddy and Krishnahantha, 1975), and they can be intensely and selectively stained with
the diaminobenzidene reaction for peroxidase (Fahimi, 1968). Despite the specificity of
this method and the clarity of the resulting electron micrographs, the origin of
peroxisomes remains a subject of controversy. Some investigators insist that their
membrane is often continuous at some point with that of the smooth endoplasmic
reticulum and that peroxisomes arise as evaginations from that organelle (Novikoff and
Shin, 1964; Essner, 1967). Others find no convincing evidence of continuity and suggest
instead that new peroxisomes arise from preexisting peroxisomes by a process of
budding. Catalase is believed to be synthesized on ribosomes and transferred directly to
the peroxisomes without involvement of the reticulum and Golgi complex (Legg and
Wood, 1970). Others observe catalase reaction product on ribosomes in the vicinity of
weakly stained, small peroxisome-like bodies that lack a distinct limiting membrane,
and suggest that catalase which is synthesized on free and bound ribosomes accumulates locally and is then segregated by development of a limiting membrane (Fahimi,
1971).
Additional support for the concept of synthesis of peroxisomal enzymes in the
cytoplasmic matrix also comes from biochemical studies which indicate that a catalase
precursor is discharged into the cytosol and subsequently transferred to the peroxisomes (Lazarow and DeDuve, 1973). Catalase has been localized on free ribosomes but
not on membrane-bound ribosomes. Thus it is the prevailing view that uricase and
catalase are transferred to the interior of the peroxisome by a posttranslational
mechanism (Goldman and Blobel, 1978). The origin of the limiting membrane is not
clear, but budding from the rough reticulum or from GERL remains a likely possibility.
Application of the cytochemical staining reaction for peroxidase has shown that, in
addition to the peroxisomes of kidney and liver, there are very large numbers of small
membrane-bounded particles 0.15 to 0.25 urn in the absorptive cells of the intestine and
in many other epithelia. Their membranes were originally reported by Novikoff-and
coworkers to be continuous with those of the smooth endoplasmic reticulum and they
were considered to be local diverticula or varicosities of the reticulum. Owing to their
small size and lack of nucleoids, it was suggested that these diminutive peroxidasepositive bodies should be designated microperoxisomes (Novikoff and Novikoff, 1972).
Other workers have confirmed their widespread occurrence, but in the absence of
reaction product in the lumen of the reticulum, their interpretation as local evaginations
of the reticulum has not gained general acceptance.
It is clear that peroxisomes occur in a broad spectrum of different sizes, with
nucleoids present in some cell types and lacking in others. As in the case of lysosomes,
their positive identification cannot be made on morphological criteria alone but requires
histochemical demonstration of one or more of their constitutent enzymes. Their
functional significance in the metabolism of cells remains obscure.
Peroxisomes are abundant in hepatic cells and were first isolated from the crude
lysosome fraction of liver homogenates. The micrographs on the facing page show their
characteristic appearance in situ (at arrows). They are generally spherical or ovoid and
have a homogeneous content of relatively low density. In the rat they usually have a
single crystalloid inclusion called the nucleoid. A nucleoid is also present in the hamster
but is a thin sheet, with a linear profile in section. Not infrequently it is folded and
presents a C or V shape profile in sections. The nucleoid consists of urate oxidase.
When present, the nucleoid is helpful in distinguishing peroxisomes from primary
lysosomes, but in some species that have no urate oxidase, the nucleoid is absent. In
those species in which nucleoids are present in the hepatic peroxisomes, they may be
absent in the peroxisomes of other organs.
Figure 280. An area of cytoplasm from a rat liver cell containing peroxisomes. (Micrograph courtesy of
Robert Bolender.)
Figure 281.
A comparable micrograph from hamster liver.
Figure 280, upper
Figure 281, lower
5 17
518
PEROXISOMES
Representative examples of microbodies or peroxisomes are shown here at higher
magnification. The plane of section may not include the nucleoid, as in the one at the
top of the figure. The great majority of nucleoids are sectioned obliquely and show only
a faint longitudinal striation. With patient examination of scores of micrographs, rare
longitudinal and transverse sections can be found. In this way the lattice of the urate
oxidase crystal in the rat peroxisome has been worked out in considerable detail.
Figure 282. Rat liver peroxisomes. (Micrograph courtesy of Daniel Friend.)
Figure 283. Rat liver peroxisome. (Micrograph courtesy of Richard Wood.)
Figure 282, upper
Figure 283, lower
5 19
PEROXISOMES
Some cell types may contain lysosomes and peroxisomes. In routine preparations,
these may be similar in size and density. But when stained with the diaminobenzidene
reaction for peroxidase activity, the dense reaction product clearly distinguishes the
peroxisomes from the lysosomes.
Figures 284 and 285. Leydig cells from boar testis stained with the cytochemical reaction for peroxidase.
Figure 284, upper
Figure 285, lower
521
PEROXISOMES
Although the function of peroxisomes is poorly understood, they appear to be
especially abundant in cells involved in cholesterol metabolism and synthesis of
steroids - liver, adrenal, ovary, and interstitium of the testis. A relationship to cholesterol metabolism is suggested by the observation that the number of hepatic peroxisomes
is dramatically increased by administration of several unrelated hypocholesterolemic
drugs.
The upper micrograph on the facing page from normal rat liver stained with the
diaminobenzidene reaction illustrates the normal size and number of peroxisomes. The
lower micrograph shows the remarkable increase after the administration of [4-chloro6-(2.3-xylidine) 2-pyrimidinylthio] acetic acid (Wy-14643).
Figure 286. Peroxidase-stained liver cytoplasm. (Micrograph courtesy of Darius Fahimi.)
Figure 287. Peroxidase stain of liver from an animal treated with Wy-14643. (Micrograph courtesy of
Janardan Reddy, from Reddy and Krishnahantha, Science 190 787-789, 1975.)
Figure 286, upper
Figure 287, lower
PEROXISOMES
Peroxisomes (microbodies), first observed in cells of the mouse proximal convoluted tubule, were described as spherical bodies with a homogeneous, finely granular
matrix. Nucleoids were not a characteristic feature of those peroxisomes. More recent
investigations of comparable organelles in the rat distinguish two types of formed
structures in their matrix-cylindrical inclusions 85 to 140 nm in diameter and large
tabular crystals varying in thickness and ranging up to 3 pm in length. Some
contain mainly crystalline inclusions, some mainly cylinders, and others contain both.
The inclusions tend to be at the periphery, and where they are crystals, they tend to
deform the organelle into geometric shapes.
The accompanying micrograph of a cell from the proximal convoluted tubule
shows a peroxisome near the cell base containing both crystals and a few circular
profiles of cylinders in cross section. Despite their unusual appearance, these organelles can be identified as peroxisomes by positive staining for catalase and a negative
reaction for acid phosphatase.
Figure 288. Proximal convoluted tubule cell from rat. (Micrograph courtesy of Michael Barrett and Paul
Heidger, from Cell and Tissue 157:283-305, 1975.)
Figure 288
PEROXISOMES
Two additional examples of peroxisomes from the proximal convoluted tubule of
rat kidney, one containing only crystals and the other containing cylindrical inclusions
seen here in transverse section.
Figures 289 and 290. Peroxisomes from the proximal convoluted tubule of rat kidney. (Micrograph
courtesy of Michael Barrett and Paul Heidger, from Cell and Tissue 157:283-305, 1975.)
Figure 289, upper
Figure 290, lower
PEROXISOMES
REFERENCES
Peroxisomes
Afzelius, B. The occurrence and structure of microbodies. A comparative study. J. Cell Biol. 265435-843,
1965.
Barrett, J. M. and P. M. Heidger. Microbodies of the rat renal proximal convoluted tubule: Ultrastructural and cytochemical investigations. Cell Tissue Res. 157:283-305, 1975.
DeDuve, C. The peroxisome: A new cytoplasmic organelle. Proc. Roy. Soc. Lond. 173:71, 1969.
DeDuve, C. and P. Baudhuin. Peroxisomes (microbodies and related particles). Physiol. Rev. 46:323-357,
1966. (Review)
DeDuve, C., H. Beaufay, P. Jacques, Y. Rahman-Li, 0. Z. Sellinger, R. Wattiaux and S. DeConnick.
Intracellular localization of catalase and of some oxidases in rat liver. Biochim. Biophys. Acta
40: 186-187, 1960.
Essner, E. Endoplasmic reticulum and the origin of microbodies in fetal mouse liver. Lab. Invest. 17:71,
1967.
Fahimi, H. D. Cytochemical localization of peroxidase activity in rat hepatic microbodies. J. Histochem.
Cytochem. 16547-550, 1968.
Fahimi, H. D. Morphogenesis of peroxisomes in rat liver. J. Cell Biol. 87A, 1971.
Gansler, H. and C. Rouiller. Modifications physiologiques et pathologiques du chondrome. Etude an
microscope klectronique. Schweitz Z. Pathol. Bakt. 19:217-243, 1956.
Goldman, B. M. and G . Blobel. Biogenesis of peroxisomes: Intracellular site of synthesis of catalase and
uricase. Proc. Nat. Acad. Sci. 753066-5070, 1978.
Hruban, Z. and M. Rechigl. Microbodies and related particles. Int. Rev. Cytol. Suppl. 1, 1969. (Review)
Hruban, Z., E . L. Vigil, A. Slesers and E. Hopkins. Microbodies. Constituent organelles of animal cells.
Lab. Invest. 27:184-191, 1972. (Review)
Hruban, Z. and H. Swift. Uricase: Localization in hepatic microbodies. Science 146:1316-1317, 1964.
Hruban, Z., Y. Mochizuki, J. R. Esterly and T. W. Wong. Some effects of hypocholesterolemic and
related agents. Fed. Proc. 29:385, 1970.
Lazarow, P. P. and C. DeDuve. The synthesis and turnover of rat liver peroxisomes. V. Intracellular
pathway of catalase synthesis. J . Cell Biol. 59507-524, 1973.
Legg, P. G. and R. L. Wood. New observations on microbodies. A cytochemical study on CPlB-treated
rat liver. J. Cell Biol. 45:118-129, 1970.
Leighton, F., B. Poole, H. Beaufay et al. Large scale separation of peroxisomes, mitochondria, and
lysosomes from the liver of rats injected with Triton WR-1339. J. Cell Biol. 37:483-513, 1968.
Novikoff, P. M. and A. B. Novikoff. Peroxisomes in absorptive cells of mammalian small intestine. J.
Cell Biol. 53532-560, 1972.
Reddy, J. K. and T. P. Krishnahantha. Hepatic peroxisome proliferation: Induction by two novel
compounds structurally unrelated to chlofibrate. Science 190:787-789, 1975.
Rhodin, J. Correlation of ultrastructural organization and function in normal and experimentally changed
proximal convoluted tubule cells of mouse kidney. A. B. Godvil, Stockholm, 1954.
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